STUDIES IN THE RESPIRATORY AND CARBOHYDRATE METABOLISM OF PLANT TISSUES
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1 Nezv Phytl. (968) 67, STUDIES IN THE RESPIRATORY AND CARBOHYDRATE METABOLISM OF PLANT TISSUES II. THE PASTEUR EFFECT IN POTATOES AND APPLES BY J. BARKER AND M. A. A. KHAN* The Btany Schl, Cambridge {Received i June 967) SUMMARY In eleven experiments with apples and ptates phsphenlpyruvate decreased during anxia in nine experiments. The data were thus, in general, in accrd with the 'lcalizatin' thery f the Pasteur effect. Of the eleven experiments, nly tw shwed the decrease in glucse6phsphate and increase in fructse diphsphate in anxia which are accepted as evidence that the 'activatininactivatin' thery is perating. The data were thus, in general, nt in accrd with the 'activatininactivatin' thery f the Pasteur effect. INTRODUCTION In varius tissues the Pasteur effect has been attributed t the lcalizatin f the glyclytic enzymes and substrates in certain parts f the cell (Lynen et al., 959; Lynen, 963; Wu and Racker, 959; Barker, Kahn and Slms, 964, 966, 967). The present paper presents data fr apples and ptates which, in general, cnfrm with the lcalizatin thery; in mst experiments the present data d nt accrd with the activatininactivatin thery, i.e. that hexkinase (HK) and phsphfructkinase (PKF) are activated in anxia and inactivated in air (Newshlme and Randle, 96; Passneau and Lwry, 962; Wu, 964). METHODS The techniques f Barker et al. (967) were used. Except where therwise stated, the wrk was dne at 5' C. The samples cnsisted f furteen r twenty apples r ptates respectively. RESULTS Apples Experiment i. Granny Smith {June 963) (Fig. i) In all experiments the samples were transferred t nitrgen at days. CO, utput (Fig. I a). In anxia, the CO, utput increased t abut 25",, abve the rateinair(parija, 928; Fidler, 948). Phsphate cmpunds (Figs. ibh). Glucse6phsphate (G6P), fructse6phsphate (PY)P), 3phsphglycerate (^PGA), 2phsphglycerate (2P(J.) and phsphtnlpyruvate decreased markedly during the first 6 hurs f anxia. In cntrast fructsc,6diphsphate (FDP) and dihydrxyacetnephsphate (DIIAP) increased. * Present address: Department f Bt;iny, Dacca L'nixersity, Dacca, Fast Pakistan. 2:;
2 2O6 J. BARKER AND M. A. A. KHAN Ctnineiit. The abve changes f phsphate cmpunds in anxia were thus, in general, similar t thse reprted previusly fr peas, rhddendrn leaves, buckwheat seedlings and yeast (Barker et al., 964, 966, 967; Burne and Ransn, 965; Effer and Ransn, 967). With very shrt perids f anxia, hwever, a different pattern f changes in the phsphate cmpunds was bserved; i.e. G6P may rise initially in anxia (Burne and Ransn, 965). j 4 (d) FDP (h)pep 4 5 O F6P 75 i (g) 2PGA b) G6P 4 ~ Is 2 f ) 3PGA 2 () CO, ;e ) DHAP Days Fig. I..Apples, Experiment i. Changes in the rate f CO2 utput (a) and in the cntents f phsphate cmpunds (bh) in air ( x x ) and in nitrgen ( ). In this and later figures the change t nitrgen was at days. CO2 utput in air ( x x ; # ). Experiment 2. BramJey's Seedling {May 963) (Fig. 2) CO2 utput (Fig. 2a). The CO, utput increased during the first day f anxia t nearly twice the air rate (Parija, 928).
3 Pasteur effect in ptates and apples 27 Phsphate cmpunds (Figs. 2bh). G6P, F6P, FDP and DHAP changed little during the first day f anxia but increased during the secnd day. In cntrast, 3PGA, 2PGA and PEP each decreased substantially during the first 2 hurs f anxia. Experiment 3. Bramley's Seedling [May 963) The changes in CO2 utput and in phsphate cmpunds were essentially similar t thse f Experiment 2 (Fig. 2). (d) FDP 5 (h )PEP 5 ~,^ % 25 cn I (c)f6p K ^ * "" (g) 2PGA r # ~ (b) G 5P I) a*.i 2 % jmr''' 6 ~ (f)3pga 2. ;;; ^ 2 e 6 ^_ (Q) CO. c ' * ar'' _ (e) DH AP Days Fig. 2.. pples, Experiment 2. See legend t Fig. i. Cmment. The changes f phsphate cmpunds in Experiments 2 and 3 thus differed frm thse f Experiment i (with a different variety f apple) in shwing decreases f the glyclytic intermediates 3PGA, 2PGA and PEP initially in anxia but differed in that there was but little change f the sugar phsphates and f DH.A.P. This pattern f behaviur resembles clsely that fr peas during very shrt perids f anxia and frms the basis fr the thery that in varius plant tissues the Pasteur effect N.p.
4 28 J. BARKER AND M. A. A. KHAN is due t a special type f lcalizatin (Barker et al., 964, 966, 967; Khan, 964). ]Ire er the changes f phsphate cmpunds in Experiments 2 and 3 d nt accrd with the thery tbat HK and PFK are activated in anxia by decreases in G6P and adensine triphsphate (ATP) and by increases f adensine diphsphate (ADP) and inrganic phsphate (P,) respectively (fr references see page 25). Fr the activatininactivatin thery t hld, FDP must increase initially and G6P decrease in anxia as ccurred in Fxpcrimcnt i; but these cmpunds d nt change in this manner in Experiments 2 and 3 nr in the data quted abve fr peas. Ptates Fxperimeut 4. Stck A (lw sugar ptates, March 963) (Fig. 3) CO^ utput and lactate (Fig. 3a). On exclusin f xygen the rate f CO, utput increased slightly but after 3 days was lwer tban the rate in air. The rate f lactate prductin increased t a maximum after 2 days. The qutient CO, +lactate in nitrgen' CO, in air was.6 and 2.8 after i and 2 days in anxia respectively. Phsphate esters (Figs. 3bh). After 6 hurs in nitrgen, G6P, F6P, 3PG., 2PGA, and PEP had already decreased. FDP and DH.P changed little initially in anxia but increased during the third day. Experiments 5 and 6. Stck A (lzv sugar ptates, Octber 962 and December 962) In Experiments 5 and 6, als with lw sugar ptates, the results were essentially similar t thse f Experiment 4. Cmment. The changes f phsphate cmpunds in anxia in experiments 46 were thus generally similar t thse reprted previusly (see page 26). The results fr ptates differ, bw ever, frm the ab e data in the absence f an initial increase t FDP in anxia; as in Experiments 2 and ^ abe, this is eidence against the activatin inacti'atin thery. Experiments 7 and 8. Stcks B and C {partly szveet ptates at i C, 'January 964 and January 965) In Experiments 7 and 8 with ptates, which were sweetening at C, the results were again similar t thse f Experiments 4, 5 and 6, except that the cntent f G6P increased initially in anxia; this increase may be due t the increase f GiP which ccurred. Cmment. An initial increase f G6P in anxia is evidence against the thery that HK and PFK are activated in anxia (see page 25). The metablic state f partly sweet ptates differs frm that f the lw sugar ptates used in Experiments 4, 5 and 6. The difference in metablic state may accunt fr the initial increase f G6P in Experiments 7 and 8. Experiments 9, and. Stcks B and C {fully szveet ptates at C February 965 and at C March lgg^and March 96s (Fig. 4) In Experiment 9 at i" C with fully sweet ptates, the behaviur f the phsphate cmpunds in anxia differed frm that in Experiments 6, 7 and 8; G6P and PEP appeared t decrease initially but then increased (Fig. 4); FDP increased initially and then decreased, while 3PGA did nt change.
5 Pastettr effect in ptates and apples 29 In Fxperiment with fully sweet ptates at C the changes in anxia were similar t thse f Experiments 7 and 8; again the increase f G6P may be related t the high cntent f GI P. Finally, in Fxperiment, als with fully sweet ptates at C, G6P and 3PGA appeared t decrease initially in anxia but then increased. FDP increased in anxia, while PFP remained at the air level initiallv but later was lwer than the amunt in air. (d DHAP h ) PEP 2 p ' t I» 4 I ' ' ''O O 5 :; a> E 8 (c) F6P V ^ ^ (q) 2PGA ( f 3PGA» _ (b )G6P Q t > r! A ^ ^ 3 (alcoj ^ L Days _ (e _ FDP r P f Fig. 3. Ptates, Experiment 4. (a) Changes in the rate f prductin f CO,, lacti' fermentatin prduct (CO, + lactate); CO, in air ( x x ), in air and in nitrgen lactic acid in air ( : :), in nitrgen (^ _); fermentatin prduct in nitrgen ( (hh) Changes in the cntents f phsphate cmpunds in air ( x x ) and in 3 3 E acid and A A), nitrgen Cmment. Of the 8 experiments with ptates, 6 experiments (i.e. 48 and ) shwed the initial decrease f PEP w hich is cnsidered t be an imprtant feature f the develpment f the Pasteur effect. In Experiment 9, PEP appeared t decrease initially and then increased, while in Experiment, PEP remained at the air level initially. Thus the data f Experiments 9 and d nt cnfrm w ith the pattern f behaviur f the phsphate esters shwn in the ther experiments with ptates (Fig. 3) and in several ther plant tissues (see page 26). We may cnclude either that the initial decrease f
6 2IO J. BARKER AND M. A. A. KHAN PFP is nt an essential feature in the develpment f the Pasteur effect, r that in Experiments 9 and, a factr increasing PEP masked the initial decrease f this cmpund, which is believed t initiate the Pasteur effect. In Experiment 9 this secnd factr wuld appear t perate after i day in anxia (Fig. 4); in Experiment the secnd factr apparently perated frm days s that n decrease in PEP was bserved. 8 (c ) GIP " r (f )PEP 5 5 (b) G6P V (e) 3PGA ~ 5 cr O (d) FDP 2 5 '^ 4 T 2 ^ 8 (a)co, 5 I I I I I Days ]"ig. 4. Ptates, Experiment 9. Changes in tlie rate f CO2 utput (a) and in the cntents f phsphate cmpunds (bh) in air ( x x ) and in nitrgen ( ). The metablic state f fully sweet ptates differs frm that f either lw sugar r partly sweet ptates. Thus the interactin f a secnd factr increasing PEP (Experiments 9 and ) may be related t the particular metablic state. Yet in Experiment, als with fully sweet ptates, the effect f a secnd factr n PEP was nt apparent. DISCUSSION Only the t mst recent theries f the mechanisms f the Pasteur effect will be cnsidered namely, the lcalizatin thery and the activatininactivatin thery. The first thery assumes a lcalized deficiency f ADP and P; under aerhic cnditins in the
7 Pasteur effect in ptates and apples 2 sluble part f the cell cytplasm resulting in a lw availability f ATP fr phsphrylatin fr glyclysis; this thery implies that ATP prduced in the mitchndria cannt be used fr glucse phsphrylatin fr glyclysis (Lynen et al., 959; Lynen, 963; Vu and Racker, 959). In a variant f the lcalizatin thery the glyclytic and sugar phsphrylating enzymes are visualized as being lcated tgether, pssibly in a special structure (Barker et al., 964, 966, 967). An essential feature f tbis variant cncept is that the rate f metablism f PEP shuld increase initially in anxia giving an increased rate f frmatin f glyclytic ATP. Indeed in all the earlier wrk with plant tissues (see page 26) the cntent f PEP decreased in anxia s that we may pstulate an increased rate f metablism f this cmpund. In the present data, PEP decreased in anxia in nine f the eleven experiments with apples and ptates. In the tw exceptinal experiments with ptates, PEP may have decreased initially in ne experiment but later increased t the air value (Experiment 9, Fig. 4); in the ther experiment, PEP appeared nt t change initially in anxia (Experiment ). As suggested abve, the usual decrease f PEP in anxia in these tw experiments may be masked by anther factr causing an increase f PEP. Mrever, in bth the exceptinal experiments the metablism f PEP must have been faster in anxia if as seems prbable, the increased carbn traffic f the Pasteur effect w as via the glyclytic pathway (Barker and Saifi, 952; Fidler, 948). Accrding t the secnd thery f the mechanism f the Pasteur effect, hexkinase and phsphfructkinase are inhibited by the high cntents f G6P and adensine triphsphate bserved aerbically; i.e. in air the high cncentratin f adensine triphsphate in the sluble part f the cytplasm inhibits phsphfructkinase and increases the cntent f glucse6phsphate s that he.xkinase is inhibited (Newshlme and Randle, 96; Passneau and Lwry, 962; Wu, 964). The reverse changes are believed t ccur in a transitin frm air t anxia tgether with activatin f phsphfructkinase because f increases in adensine di and mnphsphate and inrganic phsphate. But f the eleven experiments described abve fr apples and ptates, nly tw sbw the initial decrease f G6P and increase f FDP in anxia, accepted by the abve authrs as evidence f activatin f hexkinase and f phsphfructkinase. Thus, in general, the data f this paper supprt the lcalizatin cncept f the mechanism f the Pasteur effect. In cntrast the data are nt generally in accrd with the secnd thery, the activatininactivatin thery, f the Pasteur effect. [.I nte n the existence f a glyclytic structure. Evidence f the existence f a glyclytic structure is presented in Barker et al. (967). In further wrk, bth glyceraldehyde phsphate dehydrgenase and lactic dehydrgenase were shwn t be lcalized in the sarcplasmic rtticulum f muscle (Fahinni and Karnvsky, 966). Mrever, while the supernatant frm hnngenized liver centrifuged at, g had a high rate f glyclysis, the full rate f the riginal hmgenate was nly btained if the supernatant was added t the sediment separated by centrifuging at,^ (Le Page and Schneider, 948).] ACKNOWLEDGMENT We are grateful t Prfessr S. L. Ransn, Mr P. Curtis, Mr B. Gddard and t Mr B. Rystn fr their help.
8 22 J. BARKER AND M. A. A. KHAN REFERENCES BARKI:R, J. & SAII I, A. ". I;L (952). Studies in the respiratry and carbhydrate metablism f plant tissues.. ExpcriniLntal studies f the frmatin f carbn dixide, lactic acid, and ther prducts in ptat tubers under anaerbic cnditins. Prc. R. Sc, B, 4, 362. BARKLK, J., KHAN, M. A. A. & SOLOMOS, T. (964). Mechanism f the Pasteur effect. Nature, Lud., 2, 26. BARKHR, J.. KHAN, M. A. A. &.SOLOMOS, T. (966). Mechanism f the Pasteur effect in peas. Nuturi', Lud., 2, 547. BARKER, J., KHAN, AI. A. A. & SOLOMOS, T. (967). Studies in the respiratry and carbhydrate metablism f plant tissues. I. The mechanism f the Pasteur effect in peas. Nezv Phytl., 66, 577. BOURNE, D. T. & RANSON, S. L. (965). Respiratry metablism in detached Rhddendrn leaves. PI. PhysiL, Lunctistir, 4, 78. EEFER, V. R. & RANSON, S. L. (967). Sme effects f xygen cncentratin n levels f respiratry mtermediates in buckwheat seedlings. PL Physi!., Lancaster, 42, 53. FAHIMI, H. D. & KARNOVSK'I', M. J. (966). Cytlgical lcalisatin f tw glyclytic dehydrgenases in white skeletal muscle. J. Cell BiL, 29, 3. FiDLUR, J. C. (948). The cnserving influence f xygen n respirable substrate. Ann. Bt., N.S., 2,42. KHAN, M. A. A. (964). Studies in respiratry metablism f iif;her plants. Ph.D. thesis, Universit)' f Cambridge. LE PAGI:, CJ. A. & ScHNEiriER, V. C. (948). Centrifugal fractinatin f glyclytic enzymes in tissue hmgenates. j'. bil. Ckeni., 76, 2. LvNEN, F., HARTMAN, G., NEIIER, K. F. & ScHUEGRAF,.A. (959). In: Cibd Fundatin Sympsium n Regulatin f Cell Metablism (lid. by G. E. V. Wlstenhlme and C. M. O'Cnnr), p. 25. Lndn. LYNEN, F. (963). Cntrl Mechanisms in Respiratin and Fermentatin (Ed. by B. Wright), p New Yrk. NEWSHOI.ME, E. A. & RANDLE, P. J. (96). Regulatin f glucse uptake by muscle. 5. Effects f anxij, insulin, adrenaline and prlnged starving n cncentratins f hexse phsphates in islated rat diaphragm and perfused islated rat heart. Bichem. jf., 8, 655. P.RijA, P. (928). Analytic studies in plant respiratin. II. The respiratin f apples in nitrgen and its relatin t respiratin in air. Prc. R. Sc, B, 3, 446. PASSONEAU, T. V. & LwRY, O. H. (962). Phsphfructkinase and tbe Pasteur effect. Bichem. biphys. Res. Cmtnun., 7,. Wu, R. (964). Cntrl f glyclysis by phsphfructkinase in slices f rat liver, Nvikff hepatma and adrencarcinmas. Bichem. biphys. Res. Cmmun., 4, 79. Wu, R. & RACKER, E. (959). Regulatry mechanisms in carbhydrate metablism. IV. The Pasteur effect and crabtree effect in ascites tumur cells. ^. bil. Chem., 234, 36.
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